LABORATORY INVESTIGATION

J Neurosurg 135:136–146, 2021

Fine configuration of the dural fibrous network and

the extradural neural axis compartment in the jugular
foramen: an epoxy sheet plastination and confocal
microscopy study
Jacob D. Bond, BSc(Hons),1,2 Zhaoyang Xu, MB, MMed,1 and Ming Zhang, MB, MMed, PhD1,3
1
Department of Anatomy and 2Dunedin School of Medicine, University of Otago, Dunedin, New Zealand; and 3Department of
Anatomy, Anhui Medical University, Hefei, China

OBJECTIVE The extradural neural axis compartment (EDNAC) is an adipovenous zone that is located between the
meningeal (ML) and endosteal (EL) layers of the dura mater and has been minimally investigated in the jugular foramen
(JF) region. In this study, the authors aimed to explore the fine architecture of the EDNAC within the JF and evaluate
whether the EDNAC can be used as a component for JF compartmentalization.
METHODS A total of 46 cadaveric heads (31 male, 15 female; age range 54–96 years) and 30 dry skulls were exam-
ined in this study. Twelve of 46 cadaveric heads were plastinated as a series of transverse (7 sets), coronal (3 sets), and
sagittal (2 sets) slices and examined using stereomicroscopy and confocal microscopy. The dural entry points of the JF
cranial nerves were recorded in 34 cadaveric skulls. The volumes of the JF, intraforaminal EDNAC, and internal jugular
vein (IJV) were quantified.
RESULTS Based on constant osseous landmarks, the JF was subdivided into preforaminal, intraforaminal, and subfo-
raminal segments. The ML-derived fascial sheath along the anteromedial wall of the IJV demarcated the “venous por-
tion” and the “EDNAC portion” of the bipartite JF. The EDNAC did not surround the intraforaminal IJV and comprised an
ML-derived dural fibrous network and an adipose matrix. A fibrovenous curtain subdivided the intraforaminal EDNAC into
a small anterior column containing cranial nerve (CN) IX and the anterior condylar venous plexus and a large posterior
adipose column containing CNs X and XI. In the intraforaminal segment, the IJV occupied a slightly larger space in the
foramen (57%; p < 0.01), whereas in the subforaminal segment it occupied a space of similar size to that of the EDNAC.
CONCLUSIONS Excluding the IJV, the neurovascular structures in the JF traverse the dural fibrous network that is
dominant in the foraminal EDNAC. The results of this study will contribute to anatomical knowledge of the obscure yet
crucially important JF region, increase understanding of foraminal tumor growth and spread patterns, and facilitate the
planning and execution of surgical interventions.
https://thejns.org/doi/abs/10.3171/2020.4.JNS20811
KEYWORDS jugular foramen; extradural neural axis compartment; skull base; epoxy sheet plastination; dura
configuration; anatomy

he extradural neural axis compartment (EDNAC) is functions of the EDNAC.7–9 Understanding the configura-

T an adipovenous space sandwiched between the out-

er endosteal dural layer (EL) and inner meningeal
dural layer (ML) that extends from the orbit to the coc-
cyx.1 The primary element of the EDNAC is fat, which fre-
quently contains valveless veins and is often accompanied
by traversing peripheral nerves and vascular structures.1–6
Movement of the eye, lubrication of the dural layers during
flexion and extension of the spine, and cushioning and sup-
port of traversing nerves and vessels are all conjectured
tion of the EDNAC within the JF may provide a means to
predict the growth pattern of tumors in this area and might
help inform operative approaches.
Recently, Bernard et al. (2018) demonstrated that the
EDNAC exists in the jugular foramen (JF), and that cra-
nial nerves (CNs) IX–XI and their dural sheaths and the
distal sigmoid sinus (SS) and inferior petrosal sinus (IPS)
course within the foraminal EDNAC.6 Liang et al. (2019)
also depicted a venous plexus within the JF suspended in

ABBREVIATIONS ACV = anterior condylar vein; CN = cranial nerve; EDNAC = extradural neural axis compartment; EL = endosteal dural layer; IJV = internal jugular vein;
IPS = inferior petrosal sinus; IPV = inferior petro-occipital vein; JB = jugular bulb; JF = jugular foramen; ML = meningeal dural layer; RCL = rectus capitis lateralis; SS =
sigmoid sinus.
SUBMITTED March 16, 2020. ACCEPTED April 9, 2020.
INCLUDE WHEN CITING Published online July 3, 2020; DOI: 10.3171/2020.4.JNS20811.

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an adipose matrix.10 The EDNAC presence within the fo-
ramen was even designated as a foraminal compartment
by Bernard et al.6 Compartmentalization of the JF is con-
troversial due to its irregular morphology and the com-
plexity of its crowded contents; indeed, 4 different com-
partmental models have been proposed so far.11
At present, there is a dearth of literature concerning the
EDNAC, let alone its presence within the JF.6 It has been
reported that within the parasellar EDNAC compartment
the traversing neurovascular structures are supported by
both an adipose matrix and a dural fibrous network. This
dural network originates from the ML and continues with
neurovascular sheaths and the adipose matrix to form a
skeleton of fibrous struts within the EDNAC.12 Bernard et
al. dissected the dural layers surrounding the JF area and
defined the dural fibrous thickenings anterior and poste-
rior to CN IX as an “intrajugular ligament.”6 The intra-
jugular ligament separates CN IX from CNs X and XI
and serves as a surgical border to protect the lower cranial
nerves. However, Bernard et al. noted that it was impos-
sible to ascertain the origin and configuration of this in-
traforaminal ligament from a macroscopic perspective.6
Therefore, in the present study we aimed to explore the
configuration and distribution of the EDNAC, particularly
its dural fibrous network component, within the JF, and in
doing so test whether the EDNAC can be used as a practi-
cal element for JF compartmentation.
Methods
In this study we examined a total of 46 cadaveric heads
(31 male, 15 female; age range 54–96 years; 12 for plasti-
nation and 34 for dural entry mapping) and 30 dry skulls.
The human material used in this investigation was all
sourced, studied, and stored in accordance with the Hu-
man Tissue Act (New Zealand, 2008). Ethical approval
for this study was obtained from the University of Otago
Human Ethics Committee (Health), in conjunction with
Māori consultation being sought from the Ngāi Tahu Re-
search Consultation Committee.
Plastination
Twelve cadavers (7 male, 5 female; age range 54–87
years) were plastinated as a series of transverse (7 sets),
coronal (3 sets), and sagittal (2 sets) slices. The plastina-
tion procedure replaces the water and fat content of tis-
sues with epoxy resin, resulting in durable, transparent
slices that can be observed from both macroscopic and
microscopic perspectives and allow study in situ of the
preserved anatomy of delicate structures that might oth-
erwise be damaged or destroyed using dissection.12,13 In
nuce, the plastination method entails freezing the speci-
men at −80°C for 7 days. It is then cut into 2.5-mm-thick
serial slices, with a sectioning loss of 0.9 mm of tissue.
The slices are next dehydrated in 100% acetone at −30°C
for 4 weeks and afterward degreased in 100% acetone at
22°C–24°C for 3 weeks. Forced impregnation of the tissue
then follows and involves immersion of the slices in a vac-
uum chamber containing a mixture of epoxy resins (E12/
E1/AE20; Biodue) at 0°C for 2 days. Finally, the plasti-
nated slices are cured at 45°C–50°C for 5 days.14
Bond et al.
The prepared slices were analyzed using a Leica MZ8
stereomicroscope and Leica DFC 295 digital camera (Lei-
ca Microsystems). A corollary of the plastination process
is that bundles of collagen, elastin, and neurofilaments in
the tissue become endogenously autofluorescent at an ex-
citation wavelength of 488 nm, which can be detected us-
ing confocal microscopy.
3D Reconstruction
To help better understand and interpret the plastinated
slices, the 3D architecture of 1 left JF was reconstructed
from 32 serial ultrathin coronal sections. The skull base,
first cervical vertebra, rectus capitis lateralis (RCL) mus-
cle, and foraminal neurovascular structures were manual-
ly segmented and then reconstructed and displayed as 3D
images in Amira software (version 6.9.0, Thermo Fisher
Scientific).
Dural Entry Mapping
Sixty-eight jugular foramina from 34 cadaveric skull
bases (24 male, 10 female; age range 57–96 years) were
observed to map the dural entry points of CNs IX–XI onto
a composite meatus distribution diagram.
3D Scans
Thirty dry skulls were used as a reference for the intra-
cranial and extracranial JF bony margins. An Artec Space
Spider handheld LED optical scanner (Artec 3D) was used
to topographically scan the intracranial and extracranial
dry skull bases. 3D skull models were generated in Artec
Studio 14 Professional software.
Quantification and Statistical Analysis
Foraminal volumes of 14 jugular foramina from the 7
transverse plastinated sets were estimated by tracing the
JF area on photographs of the sets using Fiji image analy-
sis software. The JF volume was obtained by multiplying
the mean traced area by the combined thickness of the
slices containing the JF and dividing by 1000 to obtain
volume in cubic centimeters using this equation: V = Ā
× (n × 3.4)/1000, where V is the volume (cm3), Ā is the
mean area, n is the slice number, and 3.4 is the total slice
thickness (mm).
The total volumes of the foraminal EDNAC and in-
ternal jugular vein (IJV) subcomponents were estimated,
as well as their volumes within the 3 newly described
foraminal segments. A Student paired t-test was used to
examine volumetric differences between the EDNAC and
IJV in the total JF and within the 3 foraminal segments.
The mean subtotal and total JF volumes were determined
by adding the volumes of the EDNAC and IJV, and the
percentage occupation of these subcomponents at each fo-
raminal segment was calculated by dividing their respec-
tive volumes by the subtotal JF volume.
Results
Segmentation of the Jugular Foramen
Bony Landmarks
The JF was a canal-like cavity formed by the tempo-
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FIG. 1. Openings of the JF. A–D: The intracranial opening without (A) and with (B–D) the dura. The blue dotted line in panels A
and B outlines the JF, which is subdivided into anterior (aJF) and posterior (pJF) parts by the intrajugular process (IJP; red dot)
of the temporal bone (Temp) and the lateral ridge (red dot) of the jugular tubercle (JT) of the occipital bone (Occ). E: Distribution
mapping of the glossopharyngeal meatus (solid dots) and the vagal meatus (empty circles). F: The extracranial opening of the JF
(blue dotted line). The red dot marks the anterolateral point of the jugular notch of the jugular process (JP). G: A transverse plas-
tinated section at the level of the extracranial opening of the left JF, exhibiting its bipartite compartmentalization. H: A schematic
diagram of the JF shown in panel G, illustrating the basic architecture of the EDNAC portion and venous portion of the JF. The
crossed arrows indicate the orientation (A = anterior; M = medial). aJF = anterior part of the JF; CC = carotid canal; EL = endosteal
layer of the dura; FL = foramen lacerum; FO = foramen ovale; FS = fascial sheath of the IJV; FVC = fibrovenous curtain; GF =
glenoid fossa; (groove) = a groove for lower cranial nerves; HC = hypoglossal canal; IAM = internal acoustic meatus; ICA = internal
carotid artery; IJP = intrajugular process; IJV = internal jugular vein; ImS = intermeatal dural septum; IPS = inferior petrosal sinus;
IX = glossopharyngeal nerve; JF = jugular foramen; JP = jugular process; JT = jugular tubercle; ML = meningeal layer of the dura;
MP = mastoid process; OC = occipital condyle; Occ = occipital bone; PCF = posterior condylar fossa; pJF = posterior part of the
JF; POF = petro-occipital fissure; SP = styloid process; SPS = superior petrosal sulcus; SS = sigmoid sulcus; Temp = temporal
bone; VII = facial nerve; VIII = vestibulocochlear nerve; X = vagus nerve; XI = accessory nerve; XII = hypoglossal nerve. Bar = 3
mm. Copyright Ming Zhang. Published with permission. Figure is available in color online only.

ral and occipital bones and had an intracranial and an ex-
tracranial opening (Fig. 1). The intracranial opening was
connected with the petro-occipital fissure anteromedially
and the sigmoid sulcus posterolaterally and was partially
divided into 2 parts by the intrajugular process of the tem-
poral bone and the lateral ridge of the jugular tubercle of
the occipital bone (Fig. 1A). CNs IX–XI entered the ante-
rior JF after piercing the ML of the dura mater (Fig. 1B).
In the majority of the specimens (91%; 62/68 foramina),
CN IX was noted to enter the JF superiorly through the
glossopharyngeal dural meatus and CNs X and XI to en-
ter the JF inferiorly through a shared vagal dural meatus.
The CNs were separated by an intermeatal dural septum
(Fig. 1B). Two cadavers (6%; 4/68 foramina) had bilateral
presentation of a common dural meatus transmitting all
3 cranial nerves (Fig. 1C), and in 1 cadaver (3%; 2/68 fo-
ramina), each nerve entered the JF via an individual dural
meatus (Fig. 1D). The dural entry mapping demonstrated
that the glossopharyngeal dural meatus was located an-
teromedially to the intrajugular process, whereas the vagal
dural meatus was situated around the lateral ridge of the
jugular tubercle (Fig. 1E). The extracranial opening of the
JF was bordered anteriorly by the inferior margin of the
jugular fossa and posteriorly by the jugular notch, which
is an anterior free margin of the jugular process of the
occipital bone (Fig. 1F). The intrajugular process is con-
nected with the anterolateral edge of the jugular tubercle
via fibrocartilage (Fig. 1G).
Segments
The JF was subdivided into 3 segments down its length,
based on 4 constant bony landmark levels (Fig. 2A–C).

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The first bony level was at the intracranial JF opening. The
second bony level passed from the tip of the intrajugular
process, parallel to the intracranial JF opening. The third
bony level was drawn from the lateral lip of the extracra-
nial JF opening to the lateral edge of the occipital condyle
(Fig. 2B). The fourth line, from the mastoid process, also
spanned across to the lateral edge of the occipital condyle.
The areas between these levels were defined as the pre-
foraminal, intraforaminal, and subforaminal segments of
the JF (Fig. 2B).
Main Contents
The anteromedial part of the JF (Fig. 2A and D) con-
tained CNs IX–XI and the IPS, and the inferior petro-oc-
cipital vein (IPV) and anterior condylar vein (ACV) and
their confluence, which drained into the jugular bulb (JB;
Fig. 2B and E). CNs X and XI were located between the
IPS and ACV, whereas CN IX was anterolateral to the IPS
(Fig. 2B, D, and E). The posterolateral part of the JF was
predominantly occupied by the JB, with some contribu-
tion from the distal SS (Fig. 2C and F).
The EDNAC Does Not Enclose the IJV
The JB of the IJV was the continuation of the distal
SS (Fig. 3A and B). Its roof and floor were morphologi-
cally akin to a dural sinus, and the EL and ML of the dura
were indistinguishable. Below the extracranial opening of
the JF, the ML detached from the EL and contributed to
the vascular fascial sheath of the IJV (Fig. 3A, C, and D).
Within the JF, the ML contributed to the vascular fascial
sheath on the anteromedial wall of the IJV (Figs. 3B, E,
and F, and 4B and D inset) and also fanned out and con-
tinued with a dural fibrous network in the EDNAC, where
an adipose matrix coexisted (Fig. 4D inset). Thus, the
ML-derived dural fibrous sheath on the anteromedial wall
of the IJV demarcated the JF into a large posterolateral
venous portion, which contained the IJV and dura only,
and a smaller anteromedial EDNAC portion, which had
neurovascular structures embedded in the adipose matrix
and an ML-derived dural fibrous network (Fig. 1H).
Neurovascular and EDNAC Arrangement in the JF
In the preforaminal segment (Fig. 4A and B), the area
was mainly occupied by the EDNAC, in addition to the
subarachnoid space, into which CN IX and its accompa-
nied emissary veins entered. The intermeatal dural sep-
tum (Fig. 1B) bordered CN IX posteroinferiorly, and the
ML fibers detached from the EL and contributed to the
neural and vascular dural sheaths (Fig. 4B).
In the intraforaminal segment (Fig. 4C and D), the IJV
was positioned posterolaterally and occupied a slightly
larger space in the foramen (57%; p < 0.01; Table 1) than
the anteromedially positioned EDNAC, which occupied
43% of the segment (Table 1) and appeared as a quad-
rangular space containing the IPS, CNs IX–XI, and an
adipose matrix. The IPS coursed through the space and
separated CN IX anterolaterally from CNs X and XI pos-
teromedially. The ML fibers from the intrajugular pro-
cess intermingled with the fascial sheath of the IPS and
extended to the occipital tubercle (Fig. 4D inset). These
Bond et al.
ML-derived fibers and the IPS formed a fibrovenous cur-
tain that further divided the quadrangular-shaped EDNAC
into a small anterior triangular column and a large poste-
rior triangular column (Figs. 1H and 4D).
In the subforaminal segment (Fig. 4E and F), the
EDNAC occupied a space of similar size to that of the
IJV (p > 0.05; Table 1). Compared with the intraforami-
nal segment, there were 2 main changes in the EDNAC
anatomy. First, CN XII entered the EDNAC, and second,
the fibrovenous curtain and the 2 EDNAC triangular col-
umns extended inferiorly. The anterior EDNAC column
was bordered anterolaterally by a visceral nerve plexus,
which passed over the internal carotid artery and IJV and
contained CN IX. The large posterior column was bor-
dered posteromedially by the atlanto-occipital joint and
the RCL and contained CNs X–XII (Figs. 1A, 3A and B,
and 4E and F).
Discussion
With the use of novel epoxy sheet plastination technol-
ogy in combination with confocal microscopy, this study
precisely revealed the fine configuration of the dural fi-
brous network and its relationship with intraforaminal
neurovascular and adipose structures. The main findings
were the following: 1) the ML-derived vascular sheath
along the anteromedial wall of the IJV demarcates the
venous portion and the EDNAC portion of the bipartite
JF (Fig. 1H), 2) the fibrovenous curtain formed by the
ML-derived fibrous sheath and the IPS subdivides the
intraforaminal EDNAC into a small anterior and a large
posterior adipose column that separates CN IX from CNs
X and XI, and 3) the boundaries and subdivisions of the
JF can be defined by constant bony landmarks. Figure 5
is a 3D reconstruction of the JF architecture, which may
serve to illustrate and aid in conceptualization of the spa-
tial arrangement of the EDNAC and the traversing neuro-
vascular structures in the JF and their relationships with
the bony landmarks (Fig. 5A–F).
Using Bony Landmarks to Define the Boundaries and
Subdivisions of the JF
Stepwise extracranial surgical approaches to the JF
have been outlined previously by Katsuta et al. (1997),15
Wen et al. (1997),16 Rhoton (2000),17 Matsushima (2015),18
and Griessenauer et al. (2016),19 among others, but these
reports primarily describe procedures to access the JF and
stop short at the RCL. The RCL arises from the trans-
verse process of C1, inserts onto the jugular process, and
is within the subforaminal segment of the JF (Fig. 5A and
B). The subdivisions presented in this study complement
previous research by detailing the anatomy within 3 newly
described JF segments: preforaminal, intraforaminal, and
subforaminal. All 3 segments are demarcated by bony
landmarks, which are visible on medical imaging. The
subdivisions proposed in this study may have a number
of clinical applications. For instance, paragangliomas and
meningiomas of the JF often grow in an irregular manner,
and currently there is a lack of consensus on classification
(in contradistinction to schwannomas).20–23 By applying
the zoning presented herein, tumor classification could be
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Bond et al.

FIG. 2. Coronal and sagittal plastinated sections of the JF. A–C: Three adjacent coronal sections at the levels indicated by vertical dashed lines in panel
E. The 4 red dashed boundary lines in B divide the JF into preforaminal (PRE), intraforaminal (INTRA), and subforaminal (SUB) segments. D–F: Three
adjacent sagittal sections at the levels indicated by vertical dashed lines in panel C. The dashed circle in D outlines the ganglion of CN X. The crossed
arrows indicate the orientation (S = superior; M = medial; P = posterior). FIG. 2. (continued)→

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 Bond et al.

FIG. 2. ACC = anterior condylar venous confluent; ACV = anterior condylar vein; AOJ = atlanto-occipital joint; AR = arachnoid mater stained in purple
color; C1 = first cervical vertebra; ICA = internal carotid artery; IJP = intrajugular process; IJV = internal jugular vein; IPS = inferior petrosal sinus; IPV
= inferior petro-occipital vein; IX = glossopharyngeal nerve; JB = jugular bulb; JP = jugular process; JT = jugular tubercle; ML = meningeal layer of the
dura; MP = mastoid process; OC = occipital condyle; Occ = occipital bone; PCV = posterior condylar vein; RCL = rectus capitis lateralis; SP = styloid
process; SS = sigmoid sinus; Temp = temporal bone; TP = transverse process; VA = vertebral artery; VV = vertebral vein; X = vagus nerve; XI = acces-
sory nerve; XII = hypoglossal nerve. Bars = 3 mm. Copyright Ming Zhang. Published with permission. Figure is available in color online only.

based on the segment(s) occupied by the lesions within the
JF, particularly when this information is combined with
the distribution pattern of the venous and EDNAC por-
tions in the individual segments. These 3 segments may
also be used as operative references when accessing the JF
intracranially or extracranially (Fig. 5C and D).
The EDNAC as a Feature for JF Compartmentation
The presence of the EDNAC within the JF has been
designated as a foraminal compartment by Bernard et al.,
who demonstrated that CNs IX–XI and the IPS, distal SS,
and IJV and their dural sheaths course within the EDNAC
of the JF.6 Bernard et al. group the IPS and IJV within
the same “interperiosteodural compartment” and separate
CN IX from CNs X and XI by an “intrajugular ligament,”
resulting in the proposal of a 3-part compartmentation of
the JF.6,11 The findings of our study indicate that the IJV
is actually not part of the EDNAC, as there is no adipose

FIG. 3. A and B: Two adjacent sagittal plastinated sections of the JF, showing the architecture of the fascial sheath of the IJV at
the extracranial opening. A is lateral to B. C and D: Mirror confocal images of the box and dotted box, respectively, in panel A,
showing that the meningeal dura (single arrowheads) is detached from the endosteal dura (double arrowheads). E and F: Mirror
confocal images of the box and dotted box, respectively, in panel B, showing that neurovascular structures traverse the meningeal
dural fibrous network (single arrowheads) and adipose matrix (asterisks) in the anterior column (yellow dotted line) and posterior
column (red dotted line) of the EDNAC. The crossed arrows indicate the orientation (S = superior; P = posterior). ICA = internal
carotid artery; IJV = internal jugular vein; IX = glossopharyngeal nerve; JB = jugular bulb; JP = jugular process; ML = meningeal
layer of the dura; Occ = occipital bone; RCL = rectus capitis lateralis; SS = sigmoid sinus; Temp = temporal bone; v = vein; X =
vagus nerve; XI = accessory nerve. Bar = 1 mm. Copyright Ming Zhang. Published with permission. Figure is available in color
online only.

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Bond et al.

FIG. 4. Three transverse plastinated sections at the preforaminal (A), intraforaminal (C), and subforaminal (E) levels of the JF. B, D, and F are the
mirror confocal images of A, C, and E, respectively. The inset in panel D is the area of the adjacent section inferior to the box in panel D. Outlined
by the yellow and red dotted lines are the anterior and posterior columns of the EDNAC, respectively. Single arrowheads indicate the meningeal du-
ral fibrous network. Double arrowheads point to the endosteal dura. Asterisks mark the adipose tissue. The crossed arrows indicate the orientation
(A = anterior; M = medial). ACC = anterior condylar confluent; ACV = anterior condylar vein; AOJ = atlanto-occipital joint; C1 = first cervical vertebra;
ICA = internal carotid artery; IJV = internal jugular vein; IPS = inferior petrosal sinus; IPV = inferior petro-occipital vein; IX = glossopharyngeal nerve;
JB = jugular bulb; ML = meningeal layer of the dura; n = visceral nerve plexus; Occ = occipital bone; RCA = rectus capitis anterior; RCL = rectus
capitis lateralis; SAS = subarachnoid space; SH = stylohyoid muscle; SP = styloid process; Temp = temporal bone; v = vein; X = vagus nerve; XI =
accessory nerve; XII = hypoglossal nerve; Bar = 1 mm. Copyright Ming Zhang. Published with permission. Figure is available in color online only.

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TABLE 1. Volumetric analysis of the subcomponents of the JF thickenings anterior and posterior to CN IX as an intra-
Segment Mean Vol in cm 3
JF Occupation p jugular ligament and believed it may serve as a surgical
Subcomponents (no. of JF) (%) Value barrier to protect the lower cranial nerves, but the authors
noted that it was impossible to ascertain macroscopically
Preforaminal 0.039 the configuration and origin of the intrajugular ligament.6
EDNAC 0.05 ± 0.03 (14) 71% It has been reported that in the cavernous sinus, the travers-
IJV 0.02 ± 0.04 (14) 29% ing neurovascular structures are supported by an adipose
Subtotal 0.07 ± 0.04 (14)
matrix and a dural fibrous network that originates from
the ML of the dura, continues with neurovascular sheaths,
Intraforaminal 0.0091
and terminates in the adipose matrix, forming a “skele-
EDNAC 0.49 ± 0.17 (14) 43% ton frame” within the EDNAC.12 As shown in the present
IJV 0.64 ± 0.22 (14) 57% study, the EDNAC in the JF is dominated by the ML-de-
Subtotal 1.13 ± 0.35 (14) rived fibrous network. The ML fibers in the EDNAC are
Subforaminal 0.434 orientated in 2 general directions, either longitudinally
EDNAC 0.12 ± 0.05 (14) 46% along the neurovascular structures as the dural sheath of a
vessel or nerve, or transversely between the temporal and
IJV 0.14 ± 0.09 (14) 54%
occipital bones. These 2 types of ML fibers intermingle
Subtotal 0.26 ± 0.11 (14) around the IPS, superiorly connecting with the intermeatal
Total JF 0.055 septum and inferiorly extending to the fascial sheath of
EDNAC 0.66 ± 0.18 (14) 45% the ACV and confluence and the IJV. Therefore, together
IJV 0.80 ± 0.28 (14) 55% with the IPS, they are termed a fibrovenous curtain in the
Total 1.46 ± 0.39 (14) present study.
The fibrovenous curtain of the JF divides the EDNAC
Mean values are presented ± SD; p values are for comparison between the into a small anterior and a large posterior column (Fig.
mean EDNAC and IJV subcomponent volumes of the JF. 1H). The anterior EDNAC column contains CN IX and
the anterior condylar venous complex, while the posterior
EDNAC column transmits CNs X–XII. Figure 5C and D
space between the wall of the IJV and the periosteum in- highlights the RCL as a crucial landmark to access these
traforaminally. Accordingly, this observation contradicts 2 EDNAC columns extracranially. Intracranial dural map-
the inclusion of the IJV with the EDNAC in the Bernard et ping of the nerve entry points reported in this study may
al. model.6 The ML of the dura that passes over the antero- be used as the “intracranial gates of access” to these 2
medial wall of the IJV bridges between the intrajugular columns in the JF (Fig. 5E and F). Care should be taken
process of the temporal bone and the jugular tubercle of with structural generalization, and individual anatomi-
the occipital bone, and thus effectively forms a bipartite cal variation should be considered. Variations from the
foramen containing a venous and an EDNAC portion (Fig. “normal” 2-meatus dural septation (91%) to single (6%) or
1H). Except for the preforaminal segment, these 2 portions triple (3%) dural septation patterns observed in the present
occupy a space of a more or less similar size, although in study correspond to observations and classifications made
the intraforaminal segment, the venous portion is slightly by Tubbs et al. (2015).26
larger than the EDNAC portion (57% vs 43%).
The bipartite compartmentation proposed in this study Clinical Considerations of the EDNAC Configuration in
is virtually identical to the model proposed by Shapiro the JF
(1972).11,24 The main difference between the 2 proposed JF tumors are rare27 and are divided into 2 categories,
models is that the compartmentation proposed by Shapiro intrinsic (primary) tumors originating within the JF it-
was based on the EDNAC and IJV contents rather than self and extrinsic (secondary) tumors that penetrate the
the central bony JF constriction visible on radiographs. JF from neighboring areas.21,28 In order of frequency, the
An influential early proposal of JF compartmentation by main intrinsic JF tumors are glomus jugulare tumors,
Hovelacque (1934) placed the IPS and CN IX into the an- schwannomas, and meningiomas, and these can arise near
terior half, and CNs X and XI and the IJV in the posterior the IPS, within the lower cranial nerves, or from the JB.27,29
half.11,25 Yet another JF model, by Katsuta et al., assigned Metastatic tumors, chordomas, and chondrosarcomas are
an anterior part to the IPS, a middle part to all 3 cranial examples of extrinsic tumors that very infrequently invade
nerves, and a posterior compartment for the IJV.11,15 Both the JF from the clivus, the cerebellopontine angle, or the
Hovelacque and Katsuta et al. designated a separate com- foramen magnum.21,28,29 Based on the JF compartmenta-
partment for the IPS. However, the IPS constitutes a ve- tion presented herein, schwannomas and meningiomas
nous element that is prevalent throughout the EDNAC; would most likely be located in the EDNAC portion, while
therefore, as depicted in our model, the IPS should be the glomus jugular would originate within the vascular
classed along with the cranial nerves in the EDNAC and portion of the JF.29 Song et al. (2008) postulated that the
not separated from them. intraforaminal IPS may act as a barrier for tumor expan-
sion, impeding either upward encroachment of extracra-
Structural Septa Within the EDNAC of the Jugular nial tumors or downward growth of intracranial lesions.30
Foramen The intraforaminal fibrovenous curtain defined in this
Within the JF, Bernard et al. defined the dural fibrous study, in addition to limiting tumor expansion superiorly
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Bond et al.

FIG. 5. 3D images of the interior and exterior of the JF. The opacity of bony structures is not presented as 100%. A: An inferolateral
3D scan of the skull base and the first cervical vertebra, C1. The rectus capitis lateralis (RCL) origin and insertion are highlighted
in pink. B: A postero-infero-lateral view of a 3D image that was reconstructed from a series of the plastinated coronal sections and
may mimic a posterolateral surgical approach to the JF, centered at the RCL. The asterisks mark the anterior (*) and posterior (**)
parts of the EDNAC in the JF. C and D: The 3D image from the dashed box of panel B rotated 90° medially with (C) and without
(D) the internal jugular vein (IJV), RCL, and anterior part of the EDNAC (*). In panel D, (JB) indicates that the jugular bulb is inside
the JF and cannot be directly visualized from the interior. E and F: An interior view of the 3D JF image with (E) and without (F) the
sigmoid sinus (SS), jugular bulb (JB), hypoglossal nerve (XII), anterior condylar vein (ACV), and posterior part of the EDNAC (**).
The crossed arrows indicate the orientation (A = anterior; L = lateral; S = superior). C1 and C2 = first and second cervical vertebrae;
CC = carotid canal; FM = foramen magnum; HC = hypoglossal canal; ICA = internal carotid artery; IJP = intrajugular process; IJV
= internal jugular vein; IPS = inferior petrosal sinus; IX = glossopharyngeal nerve; JB = jugular bulb; JF = jugular foramen; JP =
jugular process; JT = jugular tubercle; MP = mastoid process; OC = occipital condyle; Occ = occipital bone; PG = parotid gland;
POF = petro-occipital fissure; RCL = rectus capitis lateralis; SP = styloid process; SS = sigmoid sinus; Temp = temporal bone; TF =
transverse foramen; TP = transverse process; VA = vertebral artery; VII = facial nerve; X = vagus nerve; XI = accessory nerve; XII =
hypoglossal nerve. Copyright Ming Zhang. Published with permission. Figure is available in color online only.

and inferiorly, may also restrict tumor growth to be con-
tained within its anterolateral or posteromedial EDNAC
column, depending on the tumor origin site. For example, a
schwannoma of CN IX would be contained within the an-
teromedial column, and conversely, a schwannoma of CN
X or XI would be confined to the posterolateral column.
These suggested mechanical barriers may be particularly
relevant to the tumor morphology observed in JF schwan-
nomas. Samii et al. (1995) classified JF schwannomas into
type A (with minimal JF encroachment), type B (within
the JF with an intracranial extension), type C (mainly
extracranial with a JF extension), and type D (dumbbell
shaped with both intra- and extracranial segments).20 It is
conceivable that type A and B tumors are contained by the
IPS inferiorly and type C tumors by the IPS superiorly.
The integrity of the limiting fibrovenous curtain may be
144 J Neurosurg Volume 135 • July 2021
compromised in the case of type D (dumbbell) schwanno-
mas, allowing unencumbered tumor growth and burgeon-
ing at both ends of the JF. Cases such as this demonstrate
that understanding of this vascular and dural relationship
within the JF may provide a means to predict the growth
pattern of tumors in this area and thus inform operative
approaches.
The EDNAC may communicate with the perineural tu-
mor spread (PNS) pathway. The PNS is a recognized pat-
tern of tumor dissemination occurring along the potential
space between the nerve and its coverings, e.g., the peri-
neurium and epineurium, and is associated with risk of tu-
mor recurrence and higher morbidity and mortality.31 The
epineurium is a continuation of the ML and lies between
the internal epineurium and around the external epineu-
rium nerve fascicles (or trunks). In the cavernous sinus, the

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ML-derived epineurium of the traversing cranial nerves
gradually fans out and continues with the adipose net-
work.12 Figures 3F and 4E of this study and Fig. 3E of the
Liang et al. report10 show that the adipose tissue within the
epineurium of CNs X and XI communicates freely with
the EDNAC in the JF.
Study Limitations
Two limitations were identified in this study: 1) only ca-
davers of older adults (age range 57–96 years) were used,
and 2) observational and quantitative measurements were
conducted only on a small sample. The EDNAC contains
abundant fat; therefore, fatty atrophy in specimens from
older adults may reduce EDNAC dimensions, resulting in
an evaluation of EDNAC size and volume that is not re-
flective of younger individuals. In addition to individual
variation of the intracranial dural meatuses, the compo-
nents and patterns of the anterior condylar venous com-
plex vary considerably, which may alter the configuration
of the dural fibrous network in the JF.32,33
Conclusions
This study is a systematic exploration of the EDNAC
within the JF and has confirmed that the EDNAC does not
surround the IJV. Instead, have we presented a novel bipar-
tite compartmentation of the JF and revealed that a fibro-
venous curtain in the JF further subdivides the foraminal
EDNAC into a small anterior and a large posterior col-
umn. Investigating the EDNAC within the JF is important,
as it will contribute to our knowledge of this obscure yet
crucially important anatomical region. Additionally, such
research will improve our understanding of foraminal tu-
mor growth and spread patterns and planning and execu-
tion of surgical interventions in this region.20,22
Acknowledgments
We would like to thank Robbie McPhee, Medical Illustrator
and Graphic Artist (University of Otago, Department of Anato-
my), for his artwork contributions. We are also grateful to Paddy
Cheah for scanning the skull bases and generating the 3D skull
models.
This project was funded by a University of Otago Research
Grant (reference no. 2018-2020) and the National Natural Science
Foundation of China (reference no. 81671368).
References
1. Parkinson D. Extradural neural axis compartment. J Neuro-
surg. 2000;92(4):585–588.
2. François P, Zemmoura I, Fouquet AMB, et al. Lateral sellar
angiolipoma: a tumor illustrative of the extradural compart-
ment of the neural axis. J Neurosurg. 2010;113(5):1053–1058.
3. Parkinson D. History of the extradural neural axis compart-
ment. Surg Neurol. 2000;54(6):422–431.
4. Zamboni P, Consorti G, Galeotti R, et al. Venous collateral
circulation of the extracranial cerebrospinal outflow routes.
Curr Neurovasc Res. 2009;6(3):204–212.
5. Sakka L, Gabrillargues J, Coll G. Anatomy of the spinal
meninges. Oper Neurosurg (Hagerstown). 2016;12(2):168–
188.
6. Bernard F, Zemmoura I, Cottier JP, et al. The interperiosteo-
dural concept applied to the jugular foramen and its compart-
mentalization. J Neurosurg. 2018;129(3):770–778.
Bond et al.
7. François P, Travers N, Lescanne E, et al. The interperiosteo-
dural concept applied to the perisellar compartment: a mi-
croanatomical and electron microscopic study. J Neurosurg.
2010;113(5):1045–1052.
8. François P, Lescanne E, Velut S. The dural sheath of the optic
nerve: descriptive anatomy and surgical applications. Adv
Tech Stand Neurosurg. 2011;36:187–198.
9. Xu Z, Lin G, Zhang H, et al. Three-dimensional architecture
of the neurovascular and adipose zones of the upper and
lower lumbar intervertebral foramina: an epoxy sheet plasti-
nation study. J Neurosurg Spine. 2020;32(5):722–732.
10. Liang L, Qu L, Chu X, et al. Meningeal architecture of the
jugular foramen: an anatomic study using plastinated histo-
logic sections. World Neurosurg. 2019;127:e809–e817.
11. Bond JD, Zhang M. Compartmental subdivisions of the jugu-
lar foramen: a review of the current models. World Neuro-
surg. 2020;136:49–57.
12. Liang L, Gao F, Xu Q, Zhang M. Configuration of fibrous
and adipose tissues in the cavernous sinus. PLoS One.
2014;9(2):e89182.
13. Liugan M, Xu Z, Zhang M. Reduced free communication of
the subarachnoid space within the optic canal in the human.
Am J Ophthalmol. 2017;179:25–31.
14. von Hagens G, Tiedemann K, Kriz W. The current potential
of plastination. Anat Embryol (Berl). 1987;175(4):411–421.
15. Katsuta T, Rhoton AL Jr, Matsushima T. The jugular fora-
men: microsurgical anatomy and operative approaches. Neu-
rosurgery. 1997;41(1):149–202.
16. Wen HT, Rhoton AL Jr, Katsuta T, de Oliveira E. Microsurgi-
cal anatomy of the transcondylar, supracondylar, and para-
condylar extensions of the far-lateral approach. J Neurosurg.
1997;87(4):555–585.
17. Rhoton AL Jr. Jugular foramen. Neurosurgery. 2000;47(3)
(suppl):S267–S285.
18. Matsushima T. Microsurgical anatomy of and surgical ap-
proaches to the jugular foramen. In: Microsurgical Anatomy
and Surgery of the Posterior Cranial Fossa. Springer;
2015:277–297.
19. Griessenauer CJ, McGrew B, Matusz P, et al. Surgical ap-
proaches to the jugular foramen: a comprehensive review. J
Neurol Surg B Skull Base. 2016;77(3):260–264.
20. Samii M, Babu RP, Tatagiba M, Sepehrnia A. Surgical
treatment of jugular foramen schwannomas. J Neurosurg.
1995;82(6):924–932.
21. Vogl TJ, Bisdas S. Differential diagnosis of jugular foramen
lesions. Skull Base. 2009;19(1):3–16.
22. Sutiono AB, Kawase T, Tabuse M, et al. Importance of
preserved periosteum around jugular foramen neurino-
mas for functional outcome of lower cranial nerves: ana-
tomic and clinical studies. Oper Neurosurg (Hagerstown).
2011;69:ons230–ons240.
23. Bakar B. The jugular foramen schwannomas: review
of the large surgical series. J Korean Neurosurg Soc.
2008;44(5):285–294.
24. Shapiro R. Compartmentation of the jugular foramen. J Neu-
rosurg. 1972;36(3):340–343.
25. Hovelacque A. Le crâne dans son ensemble. In: Ostéologie.
Vol. 2. Doin and Cie; 1934:155–156.
26. Tubbs RS, Griessenauer CJ, Bilal M, et al. Dural septation on
the inner surface of the jugular foramen: an anatomical study.
J Neurol Surg B Skull Base. 2015;76(3):214–217.
27. Ramina R, Maniglia JJ, Fernandes YB, et al. Jugular fora-
men tumors: diagnosis and treatment. Neurosurg Focus.
2004;17(2):E5.
28. Guinto G, Kageyama M, Trujillo-Luarca VH, et al. Nonglo-
mic tumors of the jugular foramen: differential diagnosis and
prognostic implications. World Neurosurg. 2014;82(6):1283–
1290.
29. Lustig LR, Jackler RK. The variable relationship between
J Neurosurg Volume 135 • July 2021 145
Unauthenticated | Downloaded 09/05/21 01:12 PM UTC
Bond et al.

the lower cranial nerves and jugular foramen tumors: impli-
cations for neural preservation. Am J Otol. 1996;17(4):658–
668.
30. Song MH, Lee HY, Jeon JS, et al. Jugular foramen schwan-
noma: analysis on its origin and location. Otol Neurotol.
2008;29(3):387–391.
31. Badger D, Aygun N. Imaging of perineural spread in head
and neck cancer. Radiol Clin North Am. 2017;55(1):139–149.
32. Kurata A, Suzuki S, Iwamoto K, et al. A new transvenous ap-
proach to the carotid-cavernous sinus via the inferior petro-
occipital vein. J Neurosurg. 2012;116(3):581–587.
33. Tubbs RS, Watanabe K, Loukas M, Cohen-Gadol AA.
Anatomy of the inferior petro-occipital vein and its rela-
tion to the base of the skull: application to surgical and
endovascular procedures of the skull base. Clin Anat.
2014;27(5):698–701.
Author Contributions
Conception and design: Zhang, Bond. Acquisition of data: all
authors. Analysis and interpretation of data: Zhang, Bond. Draft-
ing the article: Bond. Critically revising the article: Zhang,
Bond. Reviewed submitted version of manuscript: Zhang, Bond.
Approved the final version of the manuscript on behalf of all
authors: Zhang. Statistical analysis: Bond. Study supervision:
Zhang.
Correspondence
Ming Zhang: University of Otago, Dunedin, New Zealand. ming.
zhang@anatomy.otago.ac.nz.

Disclosures
The authors report no conflict of interest concerning the materi-
als or methods used in this study or the findings specified in this
paper.

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